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Insights Into the Genetic Basis of Predator-Induced Response in Daphnia Galeata

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Insights Into the Genetic Basis of Predator-Induced Response in Daphnia Galeata bioRxiv preprint doi: https://doi.org/10.1101/503904; this version posted June 29, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Insights into the genetic basis of predator-induced response in Daphnia galeata Verena Tams*1, Jana Helene Nickel*2, Anne Ehring2, Mathilde Cordellier2 * equal contribution 1 Universität Hamburg, Institute of Marine Ecosystem and Fishery Science, Große Elbstraße 133, 22767 Hamburg, Germany 2 Universität Hamburg, Institute of Zoology, Martin-Luther-King-Platz 3, 20146 Hamburg, Germany Corresponding author: [email protected], phone +49 (0)40-42838-3933 Abstract Phenotypic plastic responses allow organisms to rapidly adjust when facing environmental challenges - these responses comprise morphological, behavioral but also life-history changes. Alteration of life-history traits when exposed to predation risk have been reported often in the ecological and genomic model organism Daphnia. However, the molecular basis of this response is not well understood, especially in the context of fish predation. Here, we characterized the transcriptional profiles of two Daphnia galeata clonal lines with opposed life histories when exposed to fish kairomones. First, we conducted a differential gene expression, identifying a total of 125 candidate transcripts involved in the predator-induced response, uncovering substantial intra-specific variation. Second, we applied a gene co- expression network analysis to find clusters of tightly linked transcripts revealing the functional relations of transcripts underlying the predator-induced response. Our results showed that transcripts involved in remodeling of the cuticle, growth and digestion correlated with the response to environmental change in D. galeata. Furthermore, we used an orthology- based approach to gain functional information for transcripts lacking gene ontology (GO) information, as well as insights into the evolutionary conservation of transcripts. We could show that our candidate transcripts have orthologs in other Daphnia species but almost none in other arthropods. The unique combination of methods allowed us to identify candidate transcripts, their putative functions and evolutionary history associated with predator- induced responses in Daphnia. Our study opens up to the question as to whether the same molecular signature is associated fish kairomones-mediated life-history changes in other Daphnia species. Keywords: RNA-seq, predator-induced response, gene co-expression, phenotypic plasticity, Daphnia galeata 1 bioRxiv preprint doi: https://doi.org/10.1101/503904; this version posted June 29, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. widely used in ecology, evolution and Introduction ecotoxicology (e.g. Lampert 2011; Miner et Organisms are challenged al. 2012; Picado et al. 2007). Members of throughout their lives by environmental this genus link trophic levels from primary changes that have an impact on the health producers to consumers in freshwater and fitness of each individual. A given ecosystems and are, therefore, vulnerable phenotype that is advantageous in one to high predation risk (Lampert 2011). environmental setup might become Extensive shifts in behavior, morphology disadvantageous in another. In general, and life history traits have been observed organisms have two possibilities to cope in response to predation and predation with environmental changes: return to the risk. The responses induced by ecological niche by behavioral (i.e. invertebrate predators include migration) or physiological changes, or morphological changes such as the change the boundaries of their ecological formation of helmets in D. cucullata niche by genetic adaptation (Van Straalen (Agrawal et al. 1999) and D. longispina 2003.). The former is achieved at the (Brett 1992) and the formation of neck phenotypic level and described as a teeth in D. pulex (Tollrian 1995). Vertebrate phenotypic plastic response, while the predators cues have been shown to induce latter is a genetic adaptation process, behavioral changes linked to diel vertical where genotypes with a higher fitness pass migration (Cousyn et al. 2001; Effertz & von on their alleles to the next generation. Elert 2017; Hahn et al. 2019) as well as Predation is an important biotic changes in life history traits (Boersma et al. factor structuring whole communities (e.g. 1998; Effertz & von Elert 2017) in D. Aldana et al. 2016; Boaden & Kingsford magna. The specificity of such predator- 2015), maintaining species diversity (e.g. induced responses by vertebrate and Estes et al. 2011; Fine 2015) and driving invertebrate kairomones has been shown, natural selection in populations (e.g. e.g. for the D. longispina species complex Kuchta & Svensson 2014; Morgans & Ord from the Swiss lake Greifensee (Wolinska 2013). Vertebrate as well as invertebrate et al. 2007). The documented changes in aquatic predators release kairomones into life history traits included a decrease in size the surrounding water (Macháček 1991; at maturity when exposed to fish Schoeppner & Relyea 2009; Stibor 1992; kairomones and an increase when exposed Stibor & Lüning 1994). In some instances, to kairomones of the phantom midge kairomones can be detected by their prey, larvae, a predatory invertebrate of the inducing highly variable as well as genus Chaoborus. predator-specific responses to reduce their Although phenotypic plastic vulnerability. These predator-induced responses to predation risk have been responses are a textbook example of extensively studied in the ecological and phenotypic plasticity (Tollrian & Harvell genomic model organism Daphnia, their 1999) and have been reported in detail for genetic basis is not well understood a variety of Daphnia species (e.g. Boeing et (Mitchell et al. 2017). Linking predator- al. 2006; Herzog et al. 2016; Weider & induced responses to the underlying Pijanowska 1993; Yin et al. 2011). genome-wide expression patterns has Daphnia are small branchiopod been attempted from different crustaceans and are a model organism perspectives (length of exposure time, 2 bioRxiv preprint doi: https://doi.org/10.1101/503904; this version posted June 29, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. species and experimental conditions) in network analysis lies in the opportunity to Daphnia. Orsini et al. (2018) investigated correlate gene expression and external the effect of short-term exposure to fish information (Langfelder & Horvath 2008) kairomones (several hours) in D. magna, thus simplifying the process of candidate revealing no change in gene expression. genes identification. Additionally, Yet another study identified over 200 orthology analysis allows revealing differentially expressed genes in response functional roles as well as the evolutionary to invertebrate predation risk in D. pulex, history of transcripts. The degree of of which the most prominent classes of conservation of the predator-induced upregulated genes included cuticle genes, response can be estimated by finding zinc-metalloproteinases and vitellogenin orthologous genes in species having genes (Rozenberg et al. 2015). Finally, a diverged million years ago (Cornetti et al. study on D. ambigua under vertebrate 2019). We hypothesize that a common predation risk revealed ~50 responsive predator-induced response exists within genes involved in reproduction, digestion one Daphnia species at the gene and exoskeleton structure (Hales et al. expression level and that transcripts 2017). involved are evolutionary conserved among Daphnia species under vertebrate Our goal is to investigate the predation risk. genetic basis of life history shifts in response to vertebrate predation risk. Materials and methods Daphnia galeata is the ideal candidate Experimental organisms species is to address this question, since this species does not show diel vertical This study was conducted on two D. migration behavior (Stich & Lampert 1981) galeata genotypes originally hatched from or severe morphological changes in the resting eggs collected from Müggelsee presence of vertebrate predator cues even (northeast Germany). A previous study after long exposure, but diverse shifts in involving 24 genotypes (clonal lines) from life history traits under vertebrate four different lakes revealed that the predation risk (Tams et al. 2018). With a variation for some life history traits combined approach, we aim to understand increased for genotypes exposed to fish the complexity of responses to kairomones within the Müggelsee environmental changes such as those population (Tams et al. 2018), meaning a induced by predators, which are known to broader range of phenotypes were vary across Daphnia species. We applied a displayed for that life history trait. We transcriptomic approach (RNA- chose the genotypes M6 and M9 which sequencing), followed by differential gene differed in all of their life history traits and expression, gene co-expression and were at the contrasting
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